Steven A. Juliano

SPECIES INTRODUCTION AND REPLACEMENT AMONG MOSQUITOES: INTERSPECIFIC RESOURCE COMPETITION OR APPARENT COMPETITION?

Mechanisms by which an introduced container-dwelling mosquito, Aedes albopictus, may cause declines in a resident container-dwelling mosquito, Aedes aegypti, in South Florida were tested using a combination of field experiments and field observations. Field experiment 1 tested which species has a competitive advantage as larvae developing in water-filled tires. Densities and availability of resources (leaf litter, which is a substrate for microorganisms fed upon by larvae) were manipulated in a factorial design. Contrary to previous laboratory experiments, A. albopictus was clearly the superior competitor in this tire environment, maintaining positive population growth at higher combined density and lower per capita resource availability than did A. aegypti. The primary determinant of success in this experiment was survivorship to adulthood, and A. aegypti only survived well in this environment when raised alone at low density, with high resource availability. Field experiment 2 tested whether this advantage for A. albopictus resulted from apparent competition mediated by shared protozoan parasites in the genus Ascogregarina. In field experiment 2, A. albopictus larvae had moderate to high levels of parasitism, but A. aegypti larvae were virtually free from Ascogregarina in all experimental tires, implying that Ascogregarina played little or no role in producing the advantage for A. albopictus in field experiment 1. Thus, apparent competition does not appear to be necessary to account for the replacement of A. aegypti by A. albopictus. As a first step toward understanding variation in the outcome of this invasion, numbers of Aedes immatures and masses of adults from field collected pupae (indicators of the intensity of competition) were compared for three sites with known histories of invasion by A. albopictus and decline of A. aegypti. Differences among sites in both number of Aedes per container and masses of adults of both species were consistent with the hypothesis that intensity of competition varies among sites, and suggest that A. aegypti persists only at sites where interspecific competition is less intense. Resource competition among larvae appears to be sufficient to account for replacement of A. aegypti by A. albopictus in suburban and rural areas of South Florida, which may have been marginal habitats for A. aegypti.

Convergent Habitat Segregation of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in Southeastern Brazil and Florida

Abstract During the rainy season of 2001, the incidence of the dengue vectors Aedes aegypti and Ae. albopictus was examined in different habitats of two cities (Rio de Janeiro and Nova Iguaçu) in Rio de Janeiro State, Brazil, and in two cities (Palm Beach and Boca Raton) in Florida. Oviposition trap collections were performed in urban, suburban, and rural habitats in both areas. Our hypothesis that the abundances and frequencies of occurrence of Ae. aegypti and Ae albopictus are affected in opposite ways by increasing urbanization was only partially supported. City, habitat, and their interaction significantly affected the abundance of both species. Cities with high abundance of Ae. aegypti also had a high abundance of Ae. albopictus. The two species were most abundant in the cities of Rio de Janeiro state and the lowest in Boca Raton. Habitat had a significant but opposite effect on the abundances of Ae. aegypti and Ae. albopictus. In general, Ae. aegypti was most prevalent in highly urbanized areas and Ae. albopictus in rural, suburban, and vegetated urban areas in Rio de Janeiro state and Florida. However, abundances of the two species were similar in most suburban areas. Analyses of frequencies of occurrence showed an unexpected high level of co-occurrence of both species in the same oviposition trap. Despite the different geographical origins of Ae. albopictus in Brazil and the United States, the habitats used by this recent invader are remarkably similar in the two countries.

Interspecific Competition Between Two Invasive Species of Container Mosquitoes, Aedes aegypti and Aedes albopictus (Diptera: Culicidae), in Brazil

Abstract As a result of numerous successful invasions by both Aedes albopictus (Skuse) and Ades aegypti (L.), the current worldwide distributions of these mosquito species overlap. Shared larval habitats and shifts in the distribution and abundance of resident A. albopictus or A. aegypti after the establishment of the other species suggest that competitive displacement occurs. Experiments on larval competition between North American populations of the two species showed that A. albopictus has the competitive advantage under local field conditions, which apparently accounts for displacement of A. aegypti from much of the United States after the invasion of A. albopictus. The role of competition, and potential shifts of competitive advantage in different parts of their worldwide ranges are unknown, but variation due to intraspecific or environmental differences is possible. In the current study, we measured the performance of larvae of Brazilian populations of A. albopictus and A. aegypti competing under field conditions in Rio de Janeiro, Brazil. Finite rates of increase for each species were estimated and the effects of species composition, larval density, and leaf litter resource levels were determined. A. albopictus maintained positive population growth at higher combined densities and lower per capita resource availability than did A. aegypti. A. albopictus showed higher survivorship than A. aegypti under all treatments and leaf litter resource levels. These results indicate that in Brazil, just as in North America, A. albopictus is a superior larval competitor to A. aegypti when exploiting leaf litter resources. Our results further suggest that this competitive advantage for A. albopictus is likely to be independent of mosquito population origin, local environmental conditions, and local differences in the types of leaves that form the resource base of the aquatic habitats of larvae.

Precipitation and Temperature Effects on Populations of Aedes albopictus (Diptera: Culicidae): Implications for Range Expansion

Abstract We investigated how temperature and precipitation regime encountered over the life cycle of Aedes albopictus (Skuse) affects populations. Caged populations of A. albopictus were maintained at 22, 26, and 30°C. Cages were equipped with containers that served as sites for oviposition and larval development. All cages were assigned to one of three simulated precipitation regimes: (1) low fluctuation regime - water within the containers was allowed to evaporate to 90% of its maximum before being refilled, (2) high fluctuation regime - water was allowed to evaporate to 25% of its maximum before being refilled, and (3) drying regime - water was allowed to evaporate to complete container dryness before being refilled. Greater temperature and the absence of drying resulted in greater production of adults. Greater temperature in combination with drying were detrimental to adult production. These precipitation effects on adult production were absent at 22°C. Greater temperatures and drying treatments yielded higher and lower eclosion rates, respectively and, both yielded greater mortality. Development time and size of adults decreased with increased temperatures, and drying produced larger adults. Greater temperatures resulted in greater egg mortality. These results suggest that populations occurring in warmer regions are likely to produce more adults as long as containers do not dry completely. Populations in cooler regions are likely to produce fewer adults with the variability of precipitation contributing less to variation in adult production. Predicted climate change in North America is likely to extend the northern distribution of A. albopictus and to limit further its establishment in arid regions.

Species Interactions Among Larval Mosquitoes: Context Dependence Across Habitat Gradients

Biotic interactions involving mosquito larvae are context dependent, with effects of interactions on populations altered by ecological conditions. Relative impacts of competition and predation change across a gradient of habitat size and permanence. Asymmetrical competition is common and ecological context changes competitive advantage, potentially facilitating landscape-level coexistence of competitors. Predator effects on mosquito populations sometimes depend on habitat structure and on emergent effects of multiple predators, particularly interference among predators. Nonlethal effects of predators on mosquito oviposition, foraging, and life history are common, and their consequences for populations and for mosquito-borne disease are poorly understood. Context-dependent beneficial effects of detritus shredders on mosquitoes occur in container habitats, but these interactions appear to involve more than simple resource modification by shredders. Investigations of context-dependent interactions among mosquito larvae will yield greater understanding of mosquito population dynamics and provide useful model systems for testing theories of context dependence in communities.

A field test for competitive effects of Aedes albopictus on A. aegypti in South Florida: differences between sites of coexistence and exclusion?

We tested whether interspecific competition from Aedes albopictus had measurable effects on A. aegypti at the typical numbers of larval mosquitoes found in cemetery vases in south Florida. We also tested whether the effect of interspecific competition from A. albopictus on A. aegypti differed between sites where A. aegypti either persists or went extinct following invasion by A. albopictus. Similar experiments manipulating numbers of A. albopictus in cemetery vases were conducted at three sites of A. aegypti persistence and three sites where A. aegypti was apparently extinct. The experiments were done using numbers of larvae that were determined by observed numbers of larvae for each site, and with resources (leaf detritus) that accumulated in experimental vases placed into each field site. In both the early rainy season (when number of mosquito larvae was low) and the late rainy season (when number of mosquito larvae was high), there was a significant effect of treatment on developmental progress of experimental A. aegypti. In the late rainy season, when numbers of larvae were high, there was also a significant effect of treatment on survivorship of A. aegypti. However, the competition treatment × site type (A. aegypti persists vs extinct) interaction was never significant, indicating that the competitive effect of A. albopictus on A. aegypti did not differ systematically between persistence versus extinction sites. Thus, although competition from A. albopictus is strong under field conditions at all sites, we find no evidence that variation in the impact of interspecific competition is associated with coexistence or exclusion. Interspecific competition among larvae is thus a viable explanation for exclusion or reduction of A. aegypti in south Florida, but variation in the persistence of A. aegypti following invasion does not seem to be primarily a product of variation in the conditions in the aquatic environments of cemetery vases.

Invertebrate Carcasses as a Resource for Competing Aedes albopictus and Aedes aegypti (Diptera: Culicidae)

Abstract Terrestrial invertebrate carcasses are an important resource for insects developing in pitcher plants. However, little is known of the role of these carcasses in other containers, which also receive leaf fall and stemflow inputs. This experiment investigated effects of accumulated invertebrate carcasses as a resource for two competing mosquitoes, Aedes albopictus (Skuse) and Aedes aegypti (L.), whether either species differentially benefited from accumulated carcasses, and if such a benefit affected interspecific competition. First, we measured accumulation of invertebrate carcasses in standard containers at a field site. We then used a replacement series with five different species ratios at the same total density, and varied the input of invertebrate carcasses [dead Drosophila melanogaster (Meigen)] in three levels: none, the average input from our field site, or the maximum input recorded at our field site. Survivorship, development time, and mass were measured for each mosquito species as correlates of population growth, and were used to calculate a population performance index, λ′. There were strong positive effects of invertebrate carcass additions on all growth correlates and λ′. Differences in performance between species were pronounced in small or no carcass additions and absent in large inputs of invertebrate carcasses, but there was little evidence that inputs of invertebrate carcasses altered the competitive advantage in this system. These results suggest that terrestrial invertebrate carcasses may be an important resource for many types of container communities, and large accumulations of dead invertebrates may reduce resource competition between these mosquitoes, thus favoring coexistence. We propose that the total amount of resource, including accumulated invertebrate carcasses, may explain observed patterns of replacement involving these mosquitoes.

Detritus Type Alters the Outcome of Interspecific Competition Between Aedes aegypti and Aedes albopictus (Diptera: Culicidae)

Abstract Many studies of interspecific competition between Aedes albopictus (Skuse) and Aedes aegypti (L.) (Diptera: Culicidae) larvae show that Ae. albopictus are superior resource competitors to Ae. aegypti. Single-species studies indicate that growth and survival of Ae. albopictus and Ae. aegypti larvae are affected by the type of detritus present in containers, which presumably affects the amount and quality of microorganisms that the mosquito larvae consume. We tested whether different detritus types alter the intensity of larval competition by raising 10 different density/species combinations of Ae. albopictus and Ae. aegypti larvae under standard laboratory conditions, with one of four detritus types (oak, pine, grass, or insect) provided as a nutrient base. Intraspecific competitive effects on survival were present with all detritus types. Ae. albopictus survivorship was unaffected by interspecific competition in all treatments. Negative interspecific effects on Ae. aegypti survivorship were present with three of four detritus types, but absent with grass. Estimated finite rate of increase (λ’) was lower with pine detritus than with any other detritus type for both species. Furthermore, Ae. aegypti λ’ was negatively affected by high interspecific density in all detritus types except grass. Thus, our experiment confirms competitive asymmetry in favor of Ae. albopictus with oak, pine, or insect detritus, but also demonstrates that certain detritus types may eliminate interspecific competition among the larvae of these species, which may allow for stable coexistence. Such variation in competitive outcome with detritus type may help to account for observed patterns of coexistence/exclusion of Ae. albopictus and Ae. aegypti in the field.

LARVAL COMPETITION DIFFERENTIALLY AFFECTS ARBOVIRUS INFECTION IN AEDES MOSQUITOES.

Both density-mediated and trait-mediated indirect biotic interactions may be important in structuring communities. Indirect interactions in many study systems remain unexplored; in part, because they are often difficult to detect, and in many instances, have been identified empirically only when unexpected results arise. Indirect effects induced by competition may be particularly important among organisms with complex life cycles, wherein competitive effects experienced in one life stage influence species interactions in one or more subsequent stages. We determined whether species-specific effects of larval competition in the mosquitoes Aedes albopictus and Aedes aegypti have indirect effects at the adult stage, specifically testing for effects on arboviral infection with Sindbis virus (SINV). For A. albopictus, but not for A. aegypti, competition resulted in greater infection, body titer, and dissemination rates compared to low-competition conditions. Whole body titers of virus increased with adult size irrespective of competition. However, between competitive treatments, mosquitoes from low-competition conditions had greater mean size, with lower infection rates and lower whole body titers than the smaller mosquitoes from high-competition conditions. These results suggest that larval competition, common in natural mosquito populations, has important indirect effects on adults by altering mosquito-virus interactions. Such indirect effects may change transmission parameters of pathogens.

Temperature Effects on the Dynamics of Aedes albopictus (Diptera: Culicidae) Populations in the Laboratory

Abstract We investigated how constant temperatures of 22, 24, and 26°C experienced across the full life cycle affected the dynamics of caged populations of Aedes albopictus (Skuse). All cages were equipped with plastic beakers that served as sites for oviposition and larval development. We measured the per capita daily mortality and emergence rates of the adults and size of adult females, and estimated the intrinsic rate of increase (r) and asymptotic density (K) for each caged population. Populations at 26°C had greater intrinsic rates of increase and lower asymptotic densities than populations at 22 and 24°C. Populations at high temperatures initially had greater daily per capita emergence rates, and steeper declines in per capita emergence rate as density increased over the course of the experiment. There was no temperature effect on the size of adult females nor on the per capita daily mortality rate of adults. Results indicated that populations of Ae. albopictus occurring in regions with relatively high summer temperatures are likely to have high rates of population growth with populations of adults peaking early in the season. These populations may attain relatively low peak densities of adults. Populations occurring in regions with low summer temperatures are likely to experience slow, steady production of adults throughout the season with population size peaking later in the season, and may attain higher peak densities of adults. High temperature conditions, associated with climate change, may increase the rate of spread of Ae. albopictus by increasing rates of increase and by enhancing colonization due to rapid population growth.